Needle tract seeding following percutaneous irreversible electroporation for hepatocellular carcinoma

Background

Traditional ablative techniques for primary and metastatic liver tumours include radiofrequency ablation (RFA), microwave ablation (MWA), cryoablation (CA) and percutaneous ethanol injection.1 2 Indications for these (and other) locoregional interventions include single hepatocellular carcinoma (HCC) nodules ≤5 cm or up to three nodules ≤3 cm.2 Their strength lies in their ability to induce tumour necrosis with minimal hepatic parenchymal damage.2 Complications following these procedures include thermal liver injury, liver infarcts, hepatic abscesses, bile leak, haemorrhage, portal vein thrombosis, injury to adjacent organs (usually bowel, kidney or adrenal glands) and tumour seeding.1 2

Irreversible Electroporation (IRE) is a relatively novel non-thermal ablative technique, which uses electrical direct current (up to 3 kV) in order to produce irreversible pores in cell membranes, resulting in cell death.3 4 It has been used in ablation of liver, pancreatic, renal, prostate and lung tumours.3 5 It may be performed via an open, laparoscopic or percutaneous (CT or ultrasound-guided) approach.3 The advantage of IRE over thermal ablative techniques is its non-thermal mechanism of action. This property enables it to have minimal effect on collagen and elastin; hence its relatively safer use, compared with thermal ablative techniques, in ablating lesions adjacent to heat-sensitive structures, such as bile ducts, blood vessels, abdominal viscera, pancreatic ducts, neural tissue and the urinary collecting system.3 5 Contraindications include cardiac arrhythmias and pacemaker-dependent patients (due to the potential for electrical current transference to cardiac muscle).3 6 Major complications following IRE for hepatic malignancy include bleeding, abscess, cholangitis, biliary occlusion and portal vein thrombosis.1 3 5 7 8

Needle tract tumour seeding following liver malignancy ablation is a well-recognised complication of thermal ablative techniques,1 2 but is also becoming recognised following IRE.9 10 Previously described seeding locations have occurred intrahepatically or within the peritoneum.9 10 Here, we present a case of intercostal muscle seeding following percutaneous IRE for a primary HCC.

Case presentation

A man in his 70s was referred to our unit with a suspected liver malignancy. This patient’s medical history included obesity (body mass index 32 kg/m²), non-alcoholic fatty liver disease (NAFLD)-related liver cirrhosis, portal hypertension, oesophageal varices, splenomegaly, ascites, hypercholesterolaemia, Barrett’s oesophagus and type 2 diabetes mellitus. A suspicious liver lesion was initially picked up on a surveillance ultrasound as part of a yearly NAFLD follow-up programme (figure 1). His alpha-fetoprotein level was 6 kU/L (normal range 0–6 kU/L).

Figure 1

Ultrasound image indicating heterogenous mass within liver parenchyma (red arrow). LOGIQ E9, ultrasound machine used in the scanning process.

Investigations

Liver contrast (gadolinium) enhanced MRI and staging CT scans of his thorax abdomen and pelvis indicated a diagnosis of a single 2.4×3.1 cm nodule of HCC located deep in segment VI and no evidence of metastatic disease (T1a N0 M0) (figure 2). His case was discussed in the regional hepato–pancreato–biliary multidisciplinary team (HPB MDT) meeting. The lesion was not deemed suitable for surgical resection due to portal hypertension and the location of the lesion immediately adjacent to the right posterior branch of the portal vein. Thermal ablation was also deemed technically unfeasible due to proximity of the lesion to the vasculature previously mentioned, and proximity to an adjacent bowel loop. His Eastern Cooperative Oncology Group (ECOG) score was 1. His Child-Pugh score was 6 (bilirubin 22 µmol/L, albumin 36 g/L, INR 1.2, mild ascites present, no encephalopathy). CT-guided IRE was suggested as a potentially curative intervention, with simultaneous ultrasound-guided biopsy of the lesion, in order to provide a definitive tissue diagnosis for future reference. Following a fully informed discussion with the patient, highlighting the advantages and disadvantages of the treatment in detail, he consented to undergo the procedure.

Figure 2

Selected coronal (red arrow) and axial MRI sequences further illustrating likely hepatocellular carcinoma.

Treatment

Ultrasound-guided biopsy was initially performed using a 16 gauge core biopsy needle under general anaesthesia via a right anterolateral approach (histology subsequently confirmed HCC). IRE was then subsequently performed percutaneously via a right lateral intercostal approach between the 10th and 11th ribs, under CT-quidance with the NanoKnife system (AngioDynamics, Queensbury, New York, USA),4 using three needles on the target lesion placed 1.5 cm apart and parallel (figure 3). He first received 90 IRE pulses at 1200V. All needles were pulled back by 1 cm, still within the liver capsule and another 90 IRE pulses at 1200V were given. He remained stable throughout the procedure with no immediate complication.

Figure 3

Selected axial and coronal CT imaging sequences illustrating three irreversible electroporation probes via right lateral intercostal approach between 10th and 11th ribs.

Outcome and follow-up

On postprocedure day 2, the patient became tachycardic and hypotensive. A CT angiogram showed evidence of bleeding from a segment VI hepatic artery branch. This was treated with catheter angiogram and coil embolisation of a small pseudoaneurysm of a posterior segmental branch of the right hepatic artery. As part of the treatment, the patient also received a transfusion of two units of red blood cells.

He was discharged home on post-procedure day eight and enrolled onto a follow-up programme. This involved an initial triple phase CT scan of his thorax, abdomen and pelvis at 6 weeks, and then repeated imaging at 6-monthly intervals. A week after discharge, he presented with new-onset abdominal swelling. He was diagnosed with ascites which responded to medical treatment with diuretics, and was eventually discharged home after 48 hours.

At 6-week follow-up post-IRE, his ascites had vastly improved and CT triple phase liver scans showed a low density area at the site of the previous lesion, in keeping with post-IRE status (figure 4). Moreover, there was no evidence of recurrent disease in his chest, abdomen and pelvis. His alpha-fetoprotein level was 3 kU/L. At 6-month follow-up, he was still doing very well, with CT scans showing further tumour regression and post-IRE changes.

Figure 4

Axial CT imaging sequence 6 weeks post-IRE. IRE, irreversible electroporation.

At 12-month follow-up, CT triple phase liver scans indicated that the segment VI lesion remained unchanged in size, however, there was a new 2.7×2.3 cm soft-tissue nodule in the right lateral intercostal space between the 10th and 11th ribs (figure 5). This was in correspondence with where one of his IRE needles had been inserted, suggestive of needle tract tumour seeding. His alpha-fetoprotein level was now 17 kU/L. His Child-Pugh score at this point was 10 and his ECOG performance score was 2. His case was rediscussed in the HPB MDT. Surgery was not considered as an option, including resection of the intercostal nodule, due to the now multifocal nature of the disease, the patient’s deteriorating liver function and general condition, and the possibility of further microscopic disease not visible on imaging. Subsequent biopsy of the nodule confirmed a seeded deposit. The patient was referred for systemic palliative therapy with sorafenib. The disease subsequently progressed, with deteriorating liver function, pancytopenia and further enlargement of both the primary tumour lesion and the seeded deposit. He unfortunately passed away 8 months after this therapy was commenced, and 20 months after IRE was delivered.

Figure 5

Axial CT imaging sequence at 12 months post-IRE indicating intercostal seeding between 10th and 11th ribs. IRE, irreversible electroporation.